Cis-regulatory mechanisms for robust olfactory sensory neuron class-restricted odorant receptor gene expression in Drosophila

PLoS Genet. 2015 Mar 11;11(3):e1005051. doi: 10.1371/journal.pgen.1005051. eCollection 2015 Mar.

Abstract

Odor perception requires that each olfactory sensory neuron (OSN) class continuously express a single odorant receptor (OR) regardless of changes in the environment. However, little is known about the control of the robust, class-specific OR expression involved. Here, we investigate the cis-regulatory mechanisms and components that generate robust and OSN class-specific OR expression in Drosophila. Our results demonstrate that the spatial restriction of expression to a single OSN class is directed by clusters of transcription-factor DNA binding motifs. Our dissection of motif clusters of differing complexity demonstrates that structural components such as motif overlap and motif order integrate transcription factor combinations and chromatin status to form a spatially restricted pattern. We further demonstrate that changes in metabolism or temperature perturb the function of complex clusters. We show that the cooperative regulation between motifs around and within the cluster generates robust, class-specific OR expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / physiology
  • Epigenesis, Genetic
  • Gene Expression Regulation*
  • Nerve Tissue Proteins / metabolism
  • Olfactory Receptor Neurons / metabolism
  • POU Domain Factors / metabolism
  • Protein Binding
  • Receptors, Odorant / genetics*
  • Starvation
  • Temperature
  • Transcription Factors / metabolism*

Substances

  • Drosophila Proteins
  • Nerve Tissue Proteins
  • OR59B protein, Drosophila
  • POU Domain Factors
  • Pdm3 protein, Drosophila
  • Receptors, Odorant
  • Transcription Factors
  • acj6 protein, Drosophila

Grants and funding

This work was supported by The Swedish Foundation for Strategic Research, Grant number: F06-0013, (http://www.stratresearch.se/) and The Swedish Research Council, Grant number: 522-2006-6364 / K2007-66P-20436-01-04, (http://www.vr.se/), to MA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.